The oocyte is a unique cell, from which develops a complex organism comprising of germ layers, tissues and organs. In some vertebrate species it is known that the asymmetrical localization of biomolecules within the oocyte is what drives the spatial differentiation of the daughter cells required for embryogenesis. This asymmetry is first established to produce an animal-vegetal (A-V) axis which reflects the future specification of the ectoderm, mesoderm, and endoderm layers. Several pathways for localization of vegetal maternal transcripts have already been described using a few animal models. However, there is limited information about transcripts that are localized to the animal pole, even though there is accumulating evidence indicating its active establishment. Here, we performed comparative TOMO-Seq analysis on two holoblastic cleavage models: Xenopus laevis and Acipenser ruthenus oocytes during oogenesis. We found that there were many transcripts that have a temporal preference for the establishment of localization. In both models, we observed vegetal transcript gradients that were established during either the early or late oogenesis stages and transcripts that started their localization during the early stages but became more pronounced during the later stages. We found that some animal gradients were already established during the early stages, however the majority were formed during the later stages of oogenesis. Some of these temporally localized transcripts were conserved between the models, while others were species specific. Additionally, temporal de novo transcription and also degradation of transcripts within the oocyte were observed, pointing to an active remodeling of the maternal RNA pool.

Department of Developmental Biology and Morphology of Invertebrates Institute of Zoology and Biomedical Research Faculty of Biology Jagiellonian University Krakow Poland

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses University of South Bohemia in Ceske Budejovice Vodnany Czechia

Laboratory of Gene Expression Institute of Biotechnology of the Czech Academy of Sciences Vestec Czechia

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Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics 30, 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC

Bray N. L., Pimentel H., Melsted P., Pachter L. (2016). Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527. 10.1038/nbt.3519 PubMed DOI

Carotenuto R., Tussellino M. (2018). Xenopus laevis oocyte as a model for the study of the cytoskeleton. C. R. Biol. 341 (4), 219–227. 10.1016/j.crvi.2018.04.001 PubMed DOI

Chan A. P., Kloc M., Etkin L. D. (1999). Fatvg encodes a new localized RNA that uses a 25-nucleotide element (FVLE1) to localize to the vegetal cortex of Xenopus oocytes. Development 126 (22), 4943–4953. 10.1242/dev.126.22.4943 PubMed DOI

Chebanov M., Galich E. (2013). Sturgeon hatchery manual. Ankara: FAO FISHERIES AND AQUACULTURE TECHNICAL PAPER 558.

Claußen M., Lingner T., Pommerenke C., Opitz L., Salinas G., Pieler T. (2015). Global analysis of asymmetric RNA enrichment in oocytes reveals low conservation between closely related Xenopus species. Mol. Biol. Cell 26, 3777–3787. 10.1091/mbc.E15-02-0115 PubMed DOI PMC

Dettlaff T. A., Rudneva T. B. (1991). “The South African clawed toad Xenopus laevis. 231-281,”. Animal species for developmental studies. Editors Dettlaff T. A., Vassetszky S. G. (New York: Consultants Bureau; ), Vol. 2. 10.1007/978-1-4615-3654-3_9 DOI

Dettlaff T., Ginsburg A., Schmalgausen O. I. (2006). Razvitije osetrovych ryb (in Russian). Moskow: Development of sturgeon fishes, 3–223.

Dobin A., Davis C. A., Schlesinger F., Drenkow J., Zaleski C., Jha S., et al. (2013). Star: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21. 10.1093/bioinformatics/bts635 PubMed DOI PMC

Dumont J. N. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136 (2), 153–179. 10.1002/jmor.1051360203 PubMed DOI

Elinson R. P., del Pino E. M. (2012). Developmental diversity of amphibians. Wiley Interdiscip. Rev. Dev. Biol. 1 (3), 345–369. 10.1002/wdev.23 PubMed DOI PMC

Forristall C., Pondel M., Chen L., King M. L. (1995). Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development 121, 201–208. 10.1242/dev.121.1.201 PubMed DOI

Fortriede J. D., Pells T. J., Chu S., Chaturvedi P., Wang D. Z., Fisher M. E., et al. (2020). Xenbase: Deep integration of GEO & SRA RNA-seq and ChIP-seq data in a model organism database. Nucleic Acids Res. 48, D776–D782. 10.1093/nar/gkz933 PubMed DOI PMC

Gilbert S. F. (2000). Oogenesis. Developmental Biology. 6th edition. Sunderland (MA): Sinauer Associates.

Heasman J., Quarmby J., Wylie C. C. (1984). The mitochondrial cloud of Xenopus oocytes: The source of germinal granule material. Dev. Biol. 105, 458–469. 10.1016/0012-1606(84)90303-8 PubMed DOI

Houston D. W. (2013). Regulation of cell polarity and RNA localization in vertebrate oocytes. Int. Rev. Cell Mol. Biol. 306, 127–185. 10.1016/B978-0-12-407694-5.00004-3 PubMed DOI

Jagarlamudi K., Rajkovic A. (2012). Oogenesis: Transcriptional regulators and mouse models. Mol. Cell. Endocrinol. 356, 31–39. 10.1016/j.mce.2011.07.049 PubMed DOI

Kim K. H., Lee K. A. (2014). Maternal effect genes: Findings and effects on mouse embryo development. Clin. Exp. Reprod. Med. 41 (2), 47–61. 10.5653/cerm.2014.41.2.47 PubMed DOI PMC

King M. L., Zhou Y., Bubunenko M. (1999). Polarizing genetic information in the egg: RNA localization in the frog oocyte. Bioessays. 21, 546–557. 10.1002/(SICI)1521-1878(199907)21:7<546::AID-BIES3>3.0.CO;2-Z PubMed DOI

Kloc M., Etkin L. D. (1995). Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121 (2), 287–297. 10.1242/dev.121.2.287 PubMed DOI

Kloc M., Etkin L. D. (1998). Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus. Mech. Dev. 73, 95–106. 10.1016/s0925-4773(98)00041-0 PubMed DOI

Kloc M., Spohr G., Etkin L. D. (1993). Translocation of repetitive RNA sequences with the germ plasm in Xenopus oocytes. Science 10 (262), 1712–1714. 10.1126/science.7505061 PubMed DOI

Kloc M., Bilinsky S., Etkin L. (2004). The Balbiani body and germ cell determinants: 150 Years later. Curr. Top. Dev. Biol. 59, 1–36. 10.1016/S0070-2153(04)59001-4 PubMed DOI

Kopylova E., Noe L., Touzet H. (2012). SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217. 10.1093/bioinformatics/bts611 PubMed DOI

Love M. I., Huber W., Anders S. (2014). Moderated Estimation of Fold Change and Dispersion for RNA-Seq Data With DESeq2. Genome Biol. 15 (12), 1–21. PubMed PMC

Lyman-Gingerich J., Pelegri F. (2007). “Maternal factors in fish oogenesis and embryonic development,” in The fish oocyte: From basic studies to biotechnological applications. Editor Babin P. J., et al. (Springer; ), 141–174. 10.1007/978-1-4020-6235-3_6 DOI

Marlow F. L. (2010). “Oocyte polarity and the embryonic axes: The Balbiani body, an ancient oocyte asymmetry,” in Maternal control of development in vertebrates: My mother made me do it! Morgan & claypool life Sciences. Available at: https://www.ncbi.nlm.nih.gov/books/NBK53187/ . PubMed

Meneau F., Dupré A., Jessus C., Daldello E. M. (2020). Translational control of Xenopus oocyte meiosis: Toward the genomic era. Cells 9, E1502. 10.3390/cells9061502 PubMed DOI PMC

Naraine R., Abaffy P., Sidova M., Tomankova S., Pocherniaieva K., Smolik O., et al. (2020). NormQ: RNASeq normalization based on RT-qPCR derived size factors. Comput. Struct. Biotechnol. J. 18, 1173–1181. 10.1016/j.csbj.2020.05.010 PubMed DOI PMC

Naraine R., Iegorova V., Abaffy P., Franek R., Soukup V., Psenicka M., et al. (2022). Evolutionary conservation of maternal RNA localization in fishes and amphibians revealed by TOMO-Seq. Dev. Biol. 489, 146–160. 10.1016/j.ydbio.2022.06.013 PubMed DOI

National Library of Medicine(2002)National library of medicine. Available at: https://pubmed.ncbi.nlm.nih.gov/ (Accessed 2022).

Owens D. A., Butler A. M., Aguero T. H., Newman K. M., Van Booven D., King M. L. (2017). High-throughput analysis reveals novel maternal germline rnas crucial for primordial germ cell preservation and proper migration. Dev. Camb. 144 (2), 292–304. 10.1242/dev.139220 PubMed DOI PMC

Pantano L. (2021). DEGreport: Report of DEG analysis. R package version 1.28.0. Available at: lpantano.github.io/DEGreport/ .

Peshkin L., Wuhr M., Pearl E., Haas W., Freeman R. M., Jr., Gerhart J. C., et al. (2015). On the relationship of protein and mRNA dynamics in vertebrate embryonic development. Dev. Cell 35, 383–394. 10.1016/j.devcel.2015.10.010 PubMed DOI PMC

Raikova E. (1973). Ultrastructure of sturgeon oocytes at the end of previtellogenesis. II. Cytoplasmic fine structure (in Russian, English summary). Tsitologiya 15, 1352–1361. Available at: https://pubmed.ncbi.nlm.nih.gov/4361019/ . PubMed

Raikova E. (1974). Ultrastructure of the sterlet oocytes during early vitellogenesis. II. Cytoplasmic fine structure (in Russian, English summary). Tsitologiya 16, 1345–1351. Available at: https://pubmed.ncbi.nlm.nih.gov/4858119/ .

Rasar M. A., Hammes S. R. (2006). “The physiology of the Xenopus laevis ovary,”. Xenopus protocols. Editor Liu X. J. (Methods Mol Biol; ), 322, 17–30. 10.1007/978-1-59745-000-3_2 PubMed DOI

Raudvere U., Kolberg L., Kuzmin I., Arak T., Adler P., Peterson H., et al. (2019). G:Profiler: A web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 47, W191–W198. 10.1093/nar/gkz369 PubMed DOI PMC

Rodina M. (2006). Application of image analysis for the determination of nucleus position in sturgeon oocytes. J. Appl. Ichthyol. 22, 373–374. 10.1111/j.1439-0426.2007.00988.x DOI

Schnapp B. J., Arn E. A., Deshler J. O., Highett M. I. (1997). RNA localization in Xenopus oocytes. Semin. Cell Dev. Biol. 8, 529–540. 10.1006/scdb.1997.0178 PubMed DOI

Schroeder K. E., Yost H. J. (1996). Xenopus poly (A) binding protein maternal RNA is localized during oogenesis and associated with large complexes in blastula. Dev. Genet. 19, 268–276. 10.1002/(SICI)1520-6408(1996)19:3<268::AID-DVG10>3.0.CO;2-W PubMed DOI

Sekula M., Datta S., Datta S. (2017). optCluster: An R package for determining the optimal clustering algorithm. Bioinformation 13, 101–103. 10.6026/97320630013101 PubMed DOI PMC

Selman K., Wallace R. A., Sarka A., Qi X. (1993). Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morphol. 218, 203–224. 10.1002/jmor.1052180209 PubMed DOI

Session A. M., Uno Y., Kwon T., Chapman J. A., Toyoda A., Takahashi S., et al. (2016). Genome evolution in the allotetraploid frog Xenopus laevis . Nature 538, 336–343. 10.1038/nature19840 PubMed DOI PMC

Sindelka R., Sidova M., Svec D., Kubista M. (2010). Spatial expression profiles in the Xenopus laevis oocytes measured with qPCR tomography. Methods 51, 87–91. 10.1016/j.ymeth.2009.12.011 PubMed DOI

Sindelka R., Abaffy P., Qu Y., Tomankova S., Sidova M., Naraine R., et al. (2018). Asymmetric distribution of biomolecules of maternal origin in the Xenopus laevis egg and their impact on the developmental plan. Sci. Rep. 8, 8315. 10.1038/s41598-018-26592-1 PubMed DOI PMC

Song J. L., Wong J. L., Wessel G. M. (2006). Oogenesis: Single cell development and differentiation. Dev. Biol. 300, 385–405. 10.1016/j.ydbio.2006.07.041 PubMed DOI

Spence R., Gelach G., Lawrence C., Smith C. (2008). The behaviour and ecology of the zebrafish, Danio rerio . Biol. Rev. Camb. Philos. Soc. 83, 13–34. 10.1111/j.1469-185X.2007.00030.x PubMed DOI

Xu J., Gridley T. (2012). Notch signaling during oogenesis in Drosophila melanogaster . Genetics Research International. 10.1155/2012/648207 PubMed DOI PMC

Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T. L. (2012). Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinforma. 13, 134. 10.1186/1471-2105-13-134 PubMed DOI PMC

Yisraeli J. K., Sokol S., Melton D. A. (1990). A two-step model for the localization of maternal mRNA in Xenopus oocytes: Involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development 108, 289–298. 10.1242/dev.108.2.289 PubMed DOI

Zearfoss N. R., Chan A. P., Wu C. F., Kloc M., Etkin L. D. (2004). Hermes is a localized factor regulating cleavage of vegetal blastomeres in Xenopus laevis . Dev. Biol. 267, 60–71. 10.1016/j.ydbio.2003.10.032 PubMed DOI

Zelazowska M., Fopp-Bayat D. (2017). Previtellogenic and vitellogenic oocytes in ovarian follicles of cultured siberian sturgeon Acipenser baerii (chondrostei, acipenseriformes). J. Morphol. 278, 50–61. 10.1002/jmor.20618 PubMed DOI

Zelazowska M., Fopp-Bayat D. (2019). Germline cysts and asymmetry in early previtellogenic ovarian follicles in cultured albino females of sterlet Acipenser ruthenus L. 1758 (Chondrostei, Acipenseriformes). Protoplasma 256 (5), 1229–1244. 10.1007/s00709-019-01376-0 PubMed DOI PMC

Zelazowska M. (2010). Formation and structure of egg envelopes in Russian sturgeon, Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae). J. Fish. Biol. 76, 694–706. 10.1111/j.1095-8649.2009.02527.x PubMed DOI

Zelazowska M., Kilarski W., Bilinski S. M., Podder D. D., Kloc M. (2007). Balbiani cytoplasm in oocytes of a primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani body (mitochondrial cloud) of Xenopus laevis oocytes. Cell Tissue Res. 329, 137–145. 10.1007/s00441-007-0403-9 PubMed DOI

Zhang J., King L. (1996). Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development 122, 4119–4129. 10.1242/dev.122.12.4119 PubMed DOI

RNA localization during early development of the axolotl